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Freshwater mollusks and environmental assessment of Guandu River, Rio de Janeiro, Brazil

Moluscos de água doce e avaliação ambiental do rio Guandu, Rio de Janeiro, Brasil

Abstract

The Guandu River Basin is extremely important to state of Rio de Janeiro, as a water supplier of several municipalities. However, the malacological knowledge and environmental status is not well known to this basin. The aim of this paper is to present an inventory of freshwater mollusks, as well as an environmental assessment through a Rapid Assessment Protocol, of ten sampling sites at Guandu River basin in six municipalities (Piraí, Paracambi, Japeri, Seropédica, Queimados and Nova Iguaçu). Thirteen species of molusks were found, eight native (Pomacea maculata, Biomphalaria tenagophila, Gundlachia ticaga, Gundlachia radiata, Omalonyx matheroni, Diplodon ellipticus, Anodontites trapesialis and Eupera bahiensis) and five exotics (Melanoides tuberculata, Ferrissia fragilis, Physa acuta, Corbicula fluminea and Corbicula largillierti). The environmental analysis ranked most sites as “modified”. The expansion of exotic species with their associated negative effects, as well the gap in knowledge of native species calls attention to the need of future studies of biology and ecology of the species found.

Keywords:
Gastropoda; Bivalvia; Mollusca; exotic species; RAP

Resumo

A bacia do rio Guandu é de extrema importância para o estado do Rio de Janeiro, pois abastece grande parte da região metropolitana. Contudo, aspectos malacológicos e ambientais desta bacia são pouco conhecidos. O presente trabalho teve por objetivo realizar um inventário das espécies de moluscos de água doce ocorrentes na região, assim como uma avaliação ambiental através de um Protocolo de Avaliação Rápida, de dez estações de coleta na bacia do rio Guandu em seis municípios (Piraí, Paracambi, Japeri, Seropédica, Queimados e Nova Iguaçu). Foram encontradas 13 espécies, sendo oito nativas (Pomacea maculata, Biomphalaria tenagophila, Gundlachia ticaga, Gundlachia radiata, Omalonyx matheroni, Diplodon ellipticus, Anodontites trapesialis e Eupera bahiensis) e cinco exóticas (Melanoides tuberculata, Ferrissia fragilis, Physa acuta, Corbicula fluminea e Corbicula largillierti). A avaliação ambiental caracterizou a maior parte das estações de coleta como “modificado”. A dispersão das espécies exóticas e os efeitos negativos a elas associados, além da nossa falta de conhecimento sobre as espécies nativas chama a atenção para a necessidade de futuros estudos biológicos e ecológicos das espécies encontradas.

Palavras-chave:
Gastropoda; Bivalvia; Mollusca; espécies exóticas; RAP

Introduction

Few molluscan studies were conducted in Guandu River Basin. Tubbs-Filho & Vettorazzi (2012)TUBBS-FILHO, D. & VETTORAZZI, J.S. 2012. Presença do molusco bivalve Corbicula fluminea em afluentes da bacia hidrográfica do Rio Guandu. In Bacia Hidrográfica dos Rios Guandu, da Guarda e Guandu-Mirim/Comitê da Bacia Hidrográfica Guandu (D. Tubbs-Filho, J.C.O. Antunes & J.S. Vettorazzi, orgs.). INEA, Rio de Janeiro, p. 257-272. recorded the occurrence of the exotic bivalve Corbicula fluminea (Müller, 1774) in the tributaries of Ribeirão das Lajes which is an affluent of Guandu River. Lacerda et al. (2013)LACERDA, L.E.M., MIYAHIRA, I.C. & SANTOS, S.B. 2013. First record and range extension of the freshwater limpet Gundlachia radiata (Guilding, 1828) (Mollusca: Gastropoda: Planorbidae) from southeast Brazil. Checklist. 9(1):125-128. reported the first occurrence of Gundlachia radiata (Guilding, 1828) from southeast Brazil in this area. Thiengo et al. (2001)THIENGO, S.C., FERNANDEZ, M.A., BOAVENTURA, M.F., GRAULT, C.E., SILVA, H.F.R., MATTOS, A.C. & SANTOS, S.B. 2001. Freshwater Snails and Schistosomiasis Mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan Mesoregion. Mem. Inst. Oswaldo Cruz. 96 (Suppl.):177-184. reported sixteen species of limnic gastropods in the municipalities of Itaguaí, Seropédica, Queimados, Japeri, Paracambi and Nova Iguaçu, but without the information of the water body surveyed.

The concern with the conservation of natural resources is growing due to constant alteration of habitats, overuse of natural resources and introduction of exotic species, which causes loss or reduction of the diversity at all scales (Lydeard et al. 2004LYDEARD, C., COWIE, R.H., PONDER, W.F., BOGAN, A.E., BOUCHET, P., CLARK, S., CUMMINGS, K.S., FREST, T.J., GARGOMINY, O., HERBERT, D.G., HERSHLER, R., PEREZ, K., ROTH, B., SEDDON, M., STRONG, E.E. & THOMPSON, F.G. 2004. The global decline of nonmarine mollusks. BioScience. 54(4):321-330., Amaral et al. 2008AMARAL, A.C.Z., RIBEIRO, C.V., MANSUR, M.C.D., SANTOS, S.B., AVELAR, W.E.P., MATTHEWS-CASCON, H., LEITE, F.P.P., MELO, G.A.S., COELHO, P.A., BUCKUP, G.B., BUCKUP, L., VENTURA, C.R.R. & TIAGO, C.G. A situação de ameaça dos invertebrados aquáticos no Brasil. In Livro vermelho da fauna brasileira ameaçada de extinção Série Biodiversidade vol. 19 – I (A.B.M. Machado, G.M. Drummond & A.P. Paglia, orgs). Ministério do Meio Ambiente, Brasília, p. 156-301., Santos et al. 2012SANTOS, S.B., THIENGO, S.C., FERNANDEZ, M.A., MIYAHIRA, I.C., GONÇALVES, I.C.B., XIMENES, R.F., MANSUR, M.C.D. & PEREIRA, D. 2012. Espécies de moluscos límnicos invasores no Brasil. In Moluscos Límnicos invasores no Brasil - Biologia, prevenção, controle (M.C.D. Mansur, C.P. Santos, D. Pereira, I.C.P. Paz, M.L.L. Zurita, M.T.R. Rodriguez, M.V. Nehrke & P.E.A. Bergonci, eds.). Editora Redes, Porto Alegre, p. 25-49., Miyahira et al. 2012MIYAHIRA, I.C., SANTOS, S.B., MANSUR, M.C.D. & CARNEIRO, J.B. 2012. Freshwater mussels in Brazil: past, presente and future, at least, we hope they have one. American Conchologist 40(3): 16-18.). An important step for conservation is making the information of occurrence and distribution of different taxa available (Metzger & Casatti 2006METZGER, J.P. & CASATTI, L. 2006. Do diagnóstico à conservação da biodiversidade: o estado da arte do programa BIOTA/FAPESP. Biota Neotrop. 6(2): 1-23. http://www.biotaneotropica.org.br/v6n2/pt/abstract?point-view+bn00106022006 (último acesso em 12/10/2016).
http://www.biotaneotropica.org.br/v6n2/p...
). Therefore it is necessary to inventory native flora and fauna, in order to support conservation plans (Moulton et al. 2000MOULTON, T.P., MELO, G.A.S., NESSIMIAN, J., SALGADO, N.C., PAIVA, P.C., ABSALÃO, R.S., SANTOS, S.B., VELOSO, V.G. & COSTA, J.M. 2000. Invertebrados aquáticos. In A fauna ameaçada de extinção do estado do Rio de Janeiro (H.G. Bergallo, C.F.D. Rocha, M.A.S. Alves & M. van Sluys, orgs.) Editora UERJ, Rio de Janeiro, p.45-51.). Molluscan fauna were not considered in most surveys, although it is the most diverse group after arthropods, occurring in different freshwater habitats such as streams, rivers, lakes, wetlands, swamps, dams, ponds and drainage ditches, with different degrees of eutrophication. Moreover, freshwater molluscs are among the most threatened faunal group in the world (Lydeard et al. 2004LYDEARD, C., COWIE, R.H., PONDER, W.F., BOGAN, A.E., BOUCHET, P., CLARK, S., CUMMINGS, K.S., FREST, T.J., GARGOMINY, O., HERBERT, D.G., HERSHLER, R., PEREZ, K., ROTH, B., SEDDON, M., STRONG, E.E. & THOMPSON, F.G. 2004. The global decline of nonmarine mollusks. BioScience. 54(4):321-330., Bogan 2008BOGAN, A.E. 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595:139-147., Strong et al. 2008STRONG, E.E., GARGOMINY, O.G., PONDER, W.F. & BOUCHET, P. 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 595:149-166., Pereira et al. 2014PEREIRA, D., MANSUR, M.C.D., DUARTE, L.D.S., OLIVEIRA, A.S., PIMPÃO, D.M., CALLIL, C.T., ITUARTE, C., PARADA, E., PEREDO, S., DARRIGRAN, G., SCARABINO, F., CLAVIJO, C., LARA, G., MIYAHIRA, I.C., RODRIGUEZ, M.T.R. & LASSO, C. 2014. Bivalve distribution in hydrographic regions in South America: historical overview and conservation. Hydrobiologia 735(1): 15-44.).

Thus, the goals of this work were to: 1) study the freshwater mollusks diversity and distribution at the Guandu River Basin and, 2) evaluate the degree of preservation of the studied area through the application of a Rapid Assessment Protocol (RAP).

Material and methods

1. Study area and sampling

The Guandu River is formed mainly by the Ribeirão das Lajes River and the waters transposed of the Paraiba do Sul River (Tubbs-Filho & Vettorazzi 2012TUBBS-FILHO, D. & VETTORAZZI, J.S. 2012. Presença do molusco bivalve Corbicula fluminea em afluentes da bacia hidrográfica do Rio Guandu. In Bacia Hidrográfica dos Rios Guandu, da Guarda e Guandu-Mirim/Comitê da Bacia Hidrográfica Guandu (D. Tubbs-Filho, J.C.O. Antunes & J.S. Vettorazzi, orgs.). INEA, Rio de Janeiro, p. 257-272., Costa et al. 2013COSTA, M.R., MATTOS, T.M., BORGES, J.L. & ARAÚJO, F.G. 2013. Habitat preferences of common native fishes in a tropical river in Southeastern Brazil. Neotrop. ichthyol. 11(4):871-880.). The total length of the Guandu River is 108.5 km (Costa et al. 2013COSTA, M.R., MATTOS, T.M., BORGES, J.L. & ARAÚJO, F.G. 2013. Habitat preferences of common native fishes in a tropical river in Southeastern Brazil. Neotrop. ichthyol. 11(4):871-880.), flowing through the municipalities of Piraí, Paracambi, Japeri, Seropédica, Queimados, Nova Iguaçu and Rio de Janeiro, all in the state of Rio de Janeiro. In Guandu River Basin there are crops, pastures, sand extraction areas, cities, industries, hydroelectric plants and a reservoir at the responsibility of CEDAE (Companhia Estadual de Águas e Esgotos), that provide water to approximately eight million people in the metropolitan area of Rio de Janeiro (Tubbs-Filho & Vettorazzi 2012TUBBS-FILHO, D. & VETTORAZZI, J.S. 2012. Presença do molusco bivalve Corbicula fluminea em afluentes da bacia hidrográfica do Rio Guandu. In Bacia Hidrográfica dos Rios Guandu, da Guarda e Guandu-Mirim/Comitê da Bacia Hidrográfica Guandu (D. Tubbs-Filho, J.C.O. Antunes & J.S. Vettorazzi, orgs.). INEA, Rio de Janeiro, p. 257-272.).

It were performed 10 sampling sites in six municipalities: Piraí (PR1; -43.81638, -22.68165 and PR2; -43.81779, -22.68307), Paracambi (PA1; -43.80007, -22.69054 and PA2; -43.71366, -22.64109), Itaguaí (ITA; -43.78791, -22.69493), Japeri (JAP; -43.66498, -22.65561), Seropédica (SE1; -43.64508, -22.73790 and SE2; -43.63964, -22.71110), and Nova Iguaçu (NI1; -43.62473, -22.80675 and NI2; -43.62626, -22.80764) (Figure 1). The sampling sites were done at confluence of Floresta River and Ribeirão das Lajes River (PR1), Ribeirão das Lajes River (PR2 and PA1), Guandu River (PA2, ITA, JAP, SE1 and SE2) and at Guandu Reservoir (NI1 and NI2). The sampling sites have different degrees of anthropic impacts (Figure 2). PR1 and PR2, as also NI1 and NI2 are sites close together (Figure 1).

Figure 1
Studied area and the ten sampling sites at Guandu River Basin in six municipalities of the state of Rio de Janeiro.
Figure 2
Overview of the sampled sites at Guandu River Basin. A - Piraí (PR1), B - Piraí (PR2), C – Paracambi (PA1), D - Paracambi (PA2), E - Itaguaí (ITA), F - Japeri (JAP), G - Seropédica (SE1), H - Seropédica (SE2), I - Nova Iguaçu (NI1) and J - Nova Iguaçu (NI2).

1.1. Collection and analysis

The mollusks were searched in all suitable habitats, including marginal and floating vegetation, using a handled metallic scoop as described by Fernandez et al. (2008)FERNANDEZ, M.A., THIENGO, S.C. & AMARAL, R.S. 2008. Técnicas Malacológicas. In Vigilância e controle de moluscos de importância epidemiológica. (Ministério da Saúde. Departamento de vigilância epidemiológica, ed.). Editora do Ministério da Saúde, Brasília, p. 43-70.. Large freshwater mussels (Unionida) were searched in sand and muddy substrates using bare hands and feet. The search was made by three collectors during 20 minutes, totalizing one hour per sampling site. The abundance values presented are the sum of the specimens obtained in each site. The field work was done at May/2013 and January/2014.

After field work the gastropods were submitted to a parasitological test, light/dark cycle exposures test (Fernandez et al. 2008FERNANDEZ, M.A., THIENGO, S.C. & AMARAL, R.S. 2008. Técnicas Malacológicas. In Vigilância e controle de moluscos de importância epidemiológica. (Ministério da Saúde. Departamento de vigilância epidemiológica, ed.). Editora do Ministério da Saúde, Brasília, p. 43-70.). The cercariae were identified following Schell (1970)SCHELL, S. 1970. How to know the trematodes. Dubuque, WMC Brown Co. Publisher, 355pp. and preserved in AFA. Thereafter, the mollusks were anesthetized with menthol (C10H20O), sacrificed in hot water (only gastropods), soft parts were preserved in 70% ethanol and shells were preserved dry.

Mollusks were identified under a stereomicroscope according to specialized literature (e.g., Santos 2003, 2012SANTOS, S.B. 2003. Estado atual do conhecimento dos ancilídeos na América do Sul. (Mollusca, Gastropoda, Pulmonata, Basommatophora). Rev. Biol. Trop. 50(3):191-224., Simone 2006SIMONE, L.R.L. 2006. Land and freshwater mollusks of Brazil. EGB/FAPESP, São Paulo., Arruda et al. 2006ARRUDA, J.O., GOMES, S.R., RAMIREZ, R. & THOMÉ, J.W. 2006. Morfoanatomia de duas espécies do gênero Omalonyx (Mollusca, Gastropoda, Succineidae) com novo registro para Minas Gerais, Brasil. Biociências. 14(1):61-70., Lacerda et al. 2011LACERDA, L.E.M., MIYAHIRA, I.C. & SANTOS, S.B. 2011. Shell morphology of the freshwater snail Gundlachia ticaga (Gastropoda, Ancylidae) from four sites in Ilha Grande, southeastern Brazil. Zoologia. 28(3):334-342., 2013LACERDA, L.E.M., MIYAHIRA, I.C. & SANTOS, S.B. 2013. First record and range extension of the freshwater limpet Gundlachia radiata (Guilding, 1828) (Mollusca: Gastropoda: Planorbidae) from southeast Brazil. Checklist. 9(1):125-128., Miyahira et al. 2013MIYAHIRA, I.C., MANSUR, M.C.D. & SANTOS, S.B. 2013. Revision of the type specimens of Diplodon ellipticus and Diplodon expansus (Bivalvia, Unionoida, Hyriidae). Spixiana. 36(2):173-182.) and with the assistance of specialists. The classification above genus level followed Bouchet & Rocroi (2005)BOUCHET, P. & ROCROI, J.P. 2005. Classification and nomenclator of gastropods families. Malacologia. 47(1-2):1-396., Simone (2006)SIMONE, L.R.L. 2006. Land and freshwater mollusks of Brazil. EGB/FAPESP, São Paulo. and Albrecht et al. (2007)ALBRECHT, C., KUHN, K. & STREIT, B. 2007. A molecular phylogeny of Planorboidea (Gastropoda, Pulmonata). Zool. scr. 36: 27-39. for the gastropods and Graf & Cummings (2006)GRAF, D.L. & CUMMINGS, K.S. 2006. Palaeoheterodont diversity (Mollusca: Trigonioida + Unionoida): what we know and what we wish we knew about freshwater mussel evolution. Zool. j. Linn. Soc. 148:343-394. and Bieler et al. (2010)BIELER, R., CARTER, J.G. & COAN, E.V. 2010. Classification of bivalve families. Malacologia. 52(2):113-184. for bivalves. The mollusks collected were housed at Mollusk Collection of Universidade do Estado do Rio de Janeiro (UERJ).

We used the RAP developed by Callisto et al. (2002)CALLISTO, M., FERREIRA, W.R., MORENO, P., GOULART, M. & PETRUCIO, M. 2002. Aplicação de um protocolo de avaliação rápida da diversidade de habitats em atividades de ensino e pesquisa (MG-RJ). Acta limnol. bras. 14(1):91-98. to evaluate the conservation status in each sampling site at the Guandu River Basin. This protocol evaluates 22 characteristics of the water body, margins and surroundings. The final score reflects the conservation level of the site: zero to 40 points is “impacted”, 41 to 60 points is “modified” and above 61 points is “natural”.

Results

1. Species diversity, distribution and parasitological test

Thirteen species of freshwater mollusks were found: eight gastropods and five bivalves (Table 1, Figure 3). Only two genera were represented by more than one species: Gundlachia Pfeiffer, 1849 and Corbicula Megerle von Mühlfeld, 1811. Five species were exotic: C. fluminea, Corbicula largillierti (Philippi, 1844), Melanoides tuberculata (Müller, 1774), Physa acuta Draparnaud, 1805 and Ferrissia fragilis (Tyron, 1863).

Table 1
Taxonomic list of freshwater molluscs found at Guandu River basin.
Figure 3
Freshwater molluscs from Guandu River Basin. A- Pomacea maculata Perry, 1810. B – Melanoides tuberculata (Müller, 1774). C – Physa acuta Draparnaud, 1805. D – Biomphalaria tenagophila (d’Orbigny, 1835). E – Ferrissia fragilis (Tryon, 1863). F – Gundlachia radiata (Guilding, 1828). G – Gundlachia ticaga (Marcus & Marcus, 1962). H – Omalonyx matheroni (Potiez & Michaud, 1835). I – Diplodon ellipticus Spix in Wagner, 1827. J – Anodontites trapesialis (Lamarck, 1819). K – Eupera bahiensis (Spix in Wagner, 1827). L – Corbicula fluminea (Müller, 1774). M – Corbicula largillierti (Philippi, 1844). Scale bar: A, B, H, I, J, L and M = 1 cm; C, D, E, F, G and K = 1 mm.

Only the exotic species C. fluminea was found in all sampling sites. Another widespread exotic species in Guandu River Basin was M. tuberculata, missing in only one sampling site. The native species with widest distribution was Pomacea maculata Perry, 1810 found in seven sites. However, most species presented smaller distributions, restricted to three, Diplodon ellipticus Spix in Wagner, 1827, G. radiata, Gundlachia ticaga (Marcus & Marcus, 1962) and Omalonyx matheroni (Potiez & Michaud, 1835); two, F. fragilis and Anodontites trapesialis (Lamarck, 1819), or even only one sampling site, Eupera bahiensis (Spix in Wagner, 1827) (Table 2).

Table 2
Distribution and abundance of freshwater molluscs in Guandu River basin. PR – Piraí, PA – Paracambi, ITA – Itaguaí, JAP – Japeri, SE – Seropédica, NI – Nova Iguaçu. RAP - Rapid Assessment Protocol. I – Impacted, M – Modified, N – Natural.

Gundlachia ticaga is found at upstream-intermediate sites (PR1, PA1 and ITA); F. fragilis is found at intermediate sites (ITA and SE2); and G. radiata, D. ellipticus, A. trapesialis and E. bahiensis at intermediate-downstream sites (SE2, NI1 and NI2). The other species not presented a distribution limited to any specific section of the basin.

The most abundant species at Guandu River Basin was C. fluminea (431 specimens), and the less abundant was F. fragilis (3 specimens) and O. matheroni (5 specimens) (Table 2). Gundlachia radiata, D. ellipticus and E. bahiensis were restricted to few sampling sites; however these species were abundant locally.

The parasitological survey revealed only the interaction of G. ticaga with Longifurcate pharyngeate monostome cercaria (Vivax cercaria) (Trematoda: Digenea) in PR1. The exposition of the other gastropods to light/dark cycles returned negative results.

2. Habitat and environmental evaluation

All bivalves were found buried in soft sediment with some organic matter, except by E. bahiensis found attached to the roots of Eichornia sp. Ferrissia fragilis, G. radiata, G. ticaga and P. acuta were found attached to aquatic plants, decayed debris and on artificial substrates such as plastic bottles. Melanoides tuberculata and P. maculata were found over soft and hard substrates. Omalonyx matheroni was found on plants at interface water-air.

Only PR1 and PR2 were considered as “natural” on RAP; NI1 was characterized as “impacted” and the remaining sites as “modified” (Table 2). The downstream stations received the lowest scores on the RAP.

Discussion

Five exotic species were found: three freshwater snails (M. tuberculata, P. acuta and F. fragilis) and two freshwater bivalves (C. fluminea and C. largillierti); except by F. fragilis, a cryptic species that were recently reported to Brazil (Lacerda et al. 2015LACERDA, L.E.M., RICHAU, C.S., AMARAL, C.R.L.; SILVA, D.A.; CARVALHO, E.F. & SANTOS, S.B. 2015.Ferrissia fragilis (Tryon, 1863): a freshwater snail cryptic invader in Brazil revealed by morphological and molecular data. Aquat. Invasions. 10(2):157-168.), the other species can also be considered as invasive. Among these species, the most widespread and harmful are C. fluminea and M. tuberculata. Both species can cause modification of community (Santos et al. 2012SANTOS, S.B., THIENGO, S.C., FERNANDEZ, M.A., MIYAHIRA, I.C., GONÇALVES, I.C.B., XIMENES, R.F., MANSUR, M.C.D. & PEREIRA, D. 2012. Espécies de moluscos límnicos invasores no Brasil. In Moluscos Límnicos invasores no Brasil - Biologia, prevenção, controle (M.C.D. Mansur, C.P. Santos, D. Pereira, I.C.P. Paz, M.L.L. Zurita, M.T.R. Rodriguez, M.V. Nehrke & P.E.A. Bergonci, eds.). Editora Redes, Porto Alegre, p. 25-49.). Melanoides tuberculata is widespread in Brazil (Fernandez et al. 2003FERNANDEZ, M.A., THIENGO, S.C. & SIMONE, L.R.L. 2003. Distribution of the introduced freshwater snail Melanoides tuberculatus (Gastropoda: Thiaridae) in Brazil. The Nautilus. 117:78-82., Thiengo et al. 2007THIENGO, S.C., FERNANDEZ, M.A., MATTOS, A.C. & BARBOSA, A.F. 2007. Dispersão do molusco introduzidoMelanoides tuberculatus(Müller, 1774) (Gastropoda; Thiaridae) no Brasil. In Tópicos em Malacologia - ECOS do XVIII EBRAM (S.B. Santos, A.D. Pimenta, S.C. Thiengo, M.A. Fernandez, & R.S. Absalão, orgs.) SBMa, Rio de Janeiro, p.101-106., Santos et al. 2012SANTOS, S.B., THIENGO, S.C., FERNANDEZ, M.A., MIYAHIRA, I.C., GONÇALVES, I.C.B., XIMENES, R.F., MANSUR, M.C.D. & PEREIRA, D. 2012. Espécies de moluscos límnicos invasores no Brasil. In Moluscos Límnicos invasores no Brasil - Biologia, prevenção, controle (M.C.D. Mansur, C.P. Santos, D. Pereira, I.C.P. Paz, M.L.L. Zurita, M.T.R. Rodriguez, M.V. Nehrke & P.E.A. Bergonci, eds.). Editora Redes, Porto Alegre, p. 25-49.), reaching high population densities that affect native species (Freitas et al. 1987FREITAS, J.R., BEDÊ, L.C., MARCO J.R., ROCHA, L.A. & SANTOS, M.B.L. 1987. Population dynamics of aquatic snails in Pampulha reservoir. Mem. Inst. Oswaldo Cruz. 82 (Suppl. IV):299-305., Giovanelli et al. 2003GIOVANELLI, A., VIEIRA, M.V. & SILVA, C.L.P.A.C. 2003. Apparent competition through facilitation between Melanoides tuberculatus and Biomphalaria tenagophila and the control of schistosomiasis. Mem. Inst. Oswaldo Cruz. 98(3):429-431., Braga et al. 2014BRAGA, R.M.R., MIYAHIRA, I.C., LACERDA, L.E.M., GONÇALVES, I.C.B. & SANTOS, S.B. 2014. The influence of an invasive gastropod on the population dynamics of Pisidium punctiferum (Sphaeriidae) in an insular impacted stream in Rio de Janeiro, Brazil. In Medical and Applied Malacology Crossing Boundaries: Integrative Approaches to Malacology (A.R.T. Piza, L.F. Tallarico, G.O. Introíni & S.B. Santos, orgs.). Cambridge Scholars Publishing, Newcastle, p. 97-114.). Furthermore, it is the first host of different parasites that causes human diseases (Vaz et al. 1986VAZ, J.F., TELES, H.M.S., CORREA, M.A. & LEITE, S.P.S. 1986. Ocorrência no Brasil de Thiara (Melanoides) tuberculata (Muller, 1774) (Gastropoda, Prosobranchia), primeiro hospedeiro intermediário de Clonorchis sinensis (Cobbold, 1875) (Trematoda, Plathyhelmintes). Rev. Saúde Pública. 20(4):318-322., Guimarães et al. 2001GUIMARÃES, C.T., SOUZA, C.P. & SOARES, D.M. 2001. Possible competitive displacement os Planorbids by Melanoides tuberculata in Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz. 96:173-176., Pinto & Melo, 2010PINTO, H.A. & MELO, A.L. 2010. Melanoides tuberculata (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Rev. Inst. Med. Trop. São Paulo. 52(4):207-210.). However, no parasitological interaction was found for this species in Guandu River Basin.

Corbicula fluminea is a widespread species in Brazil compared to C. largillierti, that has a restrict distribution (Santos et al. 2012SANTOS, S.B., THIENGO, S.C., FERNANDEZ, M.A., MIYAHIRA, I.C., GONÇALVES, I.C.B., XIMENES, R.F., MANSUR, M.C.D. & PEREIRA, D. 2012. Espécies de moluscos límnicos invasores no Brasil. In Moluscos Límnicos invasores no Brasil - Biologia, prevenção, controle (M.C.D. Mansur, C.P. Santos, D. Pereira, I.C.P. Paz, M.L.L. Zurita, M.T.R. Rodriguez, M.V. Nehrke & P.E.A. Bergonci, eds.). Editora Redes, Porto Alegre, p. 25-49.). These observations are consistent with the situation that we found in the Guandu River Basin, where C. largillierti had a restricted distribution whereas C. fluminea was found everywhere. Previous record of C. fluminea on Guandu River Basin stated only tributaries of Ribeirão das Lajes River (Tubbs-Filho & Vettorazzi 2012TUBBS-FILHO, D. & VETTORAZZI, J.S. 2012. Presença do molusco bivalve Corbicula fluminea em afluentes da bacia hidrográfica do Rio Guandu. In Bacia Hidrográfica dos Rios Guandu, da Guarda e Guandu-Mirim/Comitê da Bacia Hidrográfica Guandu (D. Tubbs-Filho, J.C.O. Antunes & J.S. Vettorazzi, orgs.). INEA, Rio de Janeiro, p. 257-272.), but it is clear that is widespread at the basin. This last species also has caused serious economic damage to industries and power plants, due to obstruction of water pipes and competition with native bivalves (like D. ellipticus and A. trapesialis that occurs at Guandu River Basin), reducing their populations (Mansur et al. 2004MANSUR, M.C.D., CALLIL, C.T., CARODOSO, F.R. & IBARRA, J.A.A. 2004. Uma retrospectiva e mapeamento da invasão de espécies de Corbicula (Mollusca, Bivalvia, Veneroida, Corbiculidae) oriundas do sudeste asiático, na América do Sul. In Água de Lastro e Bioinvasão (J.S.V. Silva & R.C.C.L. Souza, orgs.) Editora Interciência, Rio de Janeiro, p. 39-58., Santos et al. 2012SANTOS, S.B., THIENGO, S.C., FERNANDEZ, M.A., MIYAHIRA, I.C., GONÇALVES, I.C.B., XIMENES, R.F., MANSUR, M.C.D. & PEREIRA, D. 2012. Espécies de moluscos límnicos invasores no Brasil. In Moluscos Límnicos invasores no Brasil - Biologia, prevenção, controle (M.C.D. Mansur, C.P. Santos, D. Pereira, I.C.P. Paz, M.L.L. Zurita, M.T.R. Rodriguez, M.V. Nehrke & P.E.A. Bergonci, eds.). Editora Redes, Porto Alegre, p. 25-49.). Corbicula fluminea is also the most abundant species at Guandu River Basin, as already observed by other authors in other sites (e.g., Mansur et al. 2004MANSUR, M.C.D., CALLIL, C.T., CARODOSO, F.R. & IBARRA, J.A.A. 2004. Uma retrospectiva e mapeamento da invasão de espécies de Corbicula (Mollusca, Bivalvia, Veneroida, Corbiculidae) oriundas do sudeste asiático, na América do Sul. In Água de Lastro e Bioinvasão (J.S.V. Silva & R.C.C.L. Souza, orgs.) Editora Interciência, Rio de Janeiro, p. 39-58., Santos et al. 2012SANTOS, S.B., THIENGO, S.C., FERNANDEZ, M.A., MIYAHIRA, I.C., GONÇALVES, I.C.B., XIMENES, R.F., MANSUR, M.C.D. & PEREIRA, D. 2012. Espécies de moluscos límnicos invasores no Brasil. In Moluscos Límnicos invasores no Brasil - Biologia, prevenção, controle (M.C.D. Mansur, C.P. Santos, D. Pereira, I.C.P. Paz, M.L.L. Zurita, M.T.R. Rodriguez, M.V. Nehrke & P.E.A. Bergonci, eds.). Editora Redes, Porto Alegre, p. 25-49., Pereira et al. 2014PEREIRA, D., MANSUR, M.C.D., DUARTE, L.D.S., OLIVEIRA, A.S., PIMPÃO, D.M., CALLIL, C.T., ITUARTE, C., PARADA, E., PEREDO, S., DARRIGRAN, G., SCARABINO, F., CLAVIJO, C., LARA, G., MIYAHIRA, I.C., RODRIGUEZ, M.T.R. & LASSO, C. 2014. Bivalve distribution in hydrographic regions in South America: historical overview and conservation. Hydrobiologia 735(1): 15-44., Meyer et al. 2017MEYER, A.A.N., OLIVEIRA, E., SILVA, I.S. & PRESTES, J.G. 2017. Evaluation of density of freshwater bivalves from the Environmental Protection Area (APA) of Verde River, Campo Magro, Paraná, Brazil. Pan-American Journal of Aquatic Sciences 12(1): 21-30.).

The Unionida species needs a minimum amount of nutrients in the water to survive and usually occurs in lower sections of the rivers, where there is large amount of nutrients (Pereira et. al. 2011PEREIRA, D., ARRUDA, J.O., MENEGAT, R., PORTO, M.L., SCHWARZBOLD, A. & HARTZ, S.M. 2011. Guildas tróficas, composição e distribuição de espécies de moluscos límnicos no gradiente fluvial de um riacho subtropical brasileiro. Biotemas 24(1): 21-36., 2014PEREIRA, D., MANSUR, M.C.D., DUARTE, L.D.S., OLIVEIRA, A.S., PIMPÃO, D.M., CALLIL, C.T., ITUARTE, C., PARADA, E., PEREDO, S., DARRIGRAN, G., SCARABINO, F., CLAVIJO, C., LARA, G., MIYAHIRA, I.C., RODRIGUEZ, M.T.R. & LASSO, C. 2014. Bivalve distribution in hydrographic regions in South America: historical overview and conservation. Hydrobiologia 735(1): 15-44.), as observed for D. ellipticus and A. trapesialis at Guandu River Basin. Gundlachia radiata also prefer the large section of the river, at least at Guandu River Basin (Table 2), and it is possible that have higher nutrients requirements compared to other ancylids species. The first record of this species was in this section of the river, also occurring downstream of Guandu Reservoir (Lacerda et al. 2011LACERDA, L.E.M., MIYAHIRA, I.C. & SANTOS, S.B. 2011. Shell morphology of the freshwater snail Gundlachia ticaga (Gastropoda, Ancylidae) from four sites in Ilha Grande, southeastern Brazil. Zoologia. 28(3):334-342.). It is not possible to found a reason to the restricted distributions of G. ticaga and F. fragilis based in our data.

Eupera bahiensis is recorded for the first time to the state of Rio de Janeiro and it is also the southernmost record of this species. Until now, it was found in the states of Bahia (Mansur & Meier-Brook 2000MANSUR, M.C.D. & MEIER-BROOK, C. 2000. Morphology of Eupera Bourguignat, 1854, and Byssanodonta Orbigny, 1846 with contributions to the phylogenetic systematics of Sphaeriidae and Corbiculidae (Bivalvia: Veneroida). Arch. Molluskenkd. 128(1-2):1-59.), Pernambuco (Haas 1939HAAS, F. 1939. Zur Kenntnis der Binnen-Mollusken NO-Brasiliens. Senckenbergiana. 21(3-4):254-278.), Ceará (Haas 1939HAAS, F. 1939. Zur Kenntnis der Binnen-Mollusken NO-Brasiliens. Senckenbergiana. 21(3-4):254-278.), Pará (Haas 1949 aHAAS, F. 1949a. Land- und Süßwassermollusken aus dem Amazonas-Gebiete. Arch. Molluskenkd. 78(4-6):149-156.,bHAAS, F. 1949b. On fresh water mollusk from the Amazonian region. An. Inst. Biol. 20:301-314.; Haas 1952HAAS, F. 1952. South American non-marine shells: further remarks and descriptions. Fieldiana Zool. 34(9):107-132.) and Amazonas (Haas 1949bHAAS, F. 1949b. On fresh water mollusk from the Amazonian region. An. Inst. Biol. 20:301-314.).

All other species were previously recorded to state of Rio de Janeiro. However some of them, like A. trapesialis was rarely reported. This species was recorded only one time to state of Rio de Janeiro at Juturnaíba Reservoir, municipality of Silva Jardim (Alvarenga et al. 1979ALVARENGA, L.C.F., COELHO, A.C.S., RICCI, C.N., GOMES, L.A.L. & BARROS, H.M. 1979. Resultados preliminares dos trabalhos ecológicos realizados na lagoa de Juturnaíba, município de Araruama, Estado do Rio de Janeiro, criadouro natural dos bivalves Diplodon besckeanus (Dunker, 1849) (Unionoidea; Hyriidae) e Anodontites trapesialis (Lamarck, 1819) (Muteloidea; Mycetopodidae). Anais do V Encontro de Malacologistas Brasileiros. 1:73-89.). Diplodon ellipticus is only mentioned to Paraíba do Sul River in the state of Rio de Janeiro (Morretes, 1949MORRETES, F.L. 1949. Ensaio do catálogo dos moluscos do Brasil. Arq. mus. Paranaense 7: 5-216.). These new records evidence the gaps on the distribution of freshwater mollusks species as a result of the low sampling effort.

We noticed some new municipalities occurrences compared to Thiengo et al (2001)THIENGO, S.C., FERNANDEZ, M.A., BOAVENTURA, M.F., GRAULT, C.E., SILVA, H.F.R., MATTOS, A.C. & SANTOS, S.B. 2001. Freshwater Snails and Schistosomiasis Mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan Mesoregion. Mem. Inst. Oswaldo Cruz. 96 (Suppl.):177-184.: F. fragilis to Seropédica; G. radiata to Seropédica and Nova Iguaçu; and M. tuberculata, O. matheroni and P. maculata to Paracambi and Nova Iguaçu.

We noticed only the presence of Longifurcate pharyngeate monostome cercaria (Vivax cercaria) in G. ticaga. Previous studies in the state of Rio de Janeiro have pointed out other cercaria types in this species: Gymnocephalous cercaria to the municipality of Angra dos Reis (Lopes et al. 2011LOPES, B.G., MATTOS, A.C., FERNANDEZ, M.A., LACERDA, L.E.M., MIYAHIRA I.C., SANTOS, S.B. & THIENGO, S.C. 2011. Primeiro registro de “Gymnocephalous cercaria” (TREMATODA; FASCIOLIDAE) em Gundlachia ticaga (Marcus & Marcus, 1962) (GASTROPODA; ANCYLIDAE) NO BRASIL. In XXII Encontro Brasileiro de Malacologia (C.A.O. Meirelles, org.). Sociedade Brasileira de Malacologia, Fortaleza, p.465-468.), Echinostome cercaria to Itaguaí and Vassouras (Thiengo et al. 2001THIENGO, S.C., FERNANDEZ, M.A., BOAVENTURA, M.F., GRAULT, C.E., SILVA, H.F.R., MATTOS, A.C. & SANTOS, S.B. 2001. Freshwater Snails and Schistosomiasis Mansoni in the State of Rio de Janeiro, Brazil: I - Metropolitan Mesoregion. Mem. Inst. Oswaldo Cruz. 96 (Suppl.):177-184.) and Nova Friburgo (Thiengo et al. 2002THIENGO, S.C., FERNANDEZ, M.A., BOAVENTURA, M.F., SANTOS, S.B. & MATTOS, A.C. 2002. Freshwater Snails and Schistosomiasis Mansoni in the State of Rio de Janeiro, Brazil: II – Centro Fluminense Mesoregion. Mem. Inst. Oswaldo Cruz. 96 (Suppl.):177-184.). The final host of longifurcate pharyngeate monostome cercaria are birds and mammals (Pinto & Melo 2013PINTO, H.A. & MELO, A.L. 2013. Larvas de trematódeos em moluscos do Brasil: panorama e perspectivas após um século de estudos. Rev. Patol. Trop. 42(4): 369-386.).

The RAP classification identified the most upstream collecting sites (PR1 and PR2) as natural environments. In PR1 were found more species than in PR2 (Table 2) due the greater environmental heterogeneity (more habitats available). In PR1 there are more macrophytes and some side pools, habitats for O. matheroni and G. ticaga. As the Guandu River flows across the cities of Paracambi, Itaguaí, Japeri, Seropédica and Nova Iguaçu, receives domestic and industrial sewage and margins are sharply modified. NI2 was the richest in freshwater molluscs species, and also one of the most clearly anthropized. However, it was on a small bay near the main channel of the river, thus with a good water renovation. In NI1, near to NI2, with same habitats available (soft and hard substrates, as also rooted and floating macrophytes) but with more organic input and less water circulation sustained fewer species (Table 2).

In a dense populated area, in the metropolitan area of Rio de Janeiro, we found new municipalities records, and even a new record to the state of Rio de Janeiro. The dominance and wide distribution of M. tuberculata and C. fluminea in almost all sampling sites, emphasizes the need for a continuous monitoring and control of the spread of exotic species. Also, biological and ecological aspects of native species must be studied to support conservation strategies and reduce the effects of exotic species.

Acknowledgements

We would like to thank to J. Arruda (FZB-RS), S. Thiengo (Fiocruz-RJ) and M.C.D. Mansur (UFRGS) for species identification; Maria Regiana Salgado de Mello for the help with curatorial work; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support to SBS (CNPq/PROTAX 562291/2010-5) and Doctoral scholarships to LEML and ICM ; to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for Master scholarships to ICBG, JBC, MCV and JLO; Instituto Chico Mendes de Conservação da Biodiversidade for the licenses (63407-4 to ICM and 10812-1 to SBS); and to the two anonymous reviewers that improved this manuscript.

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    14 Mar 2017
  • Reviewed
    07 Aug 2017
  • Accepted
    09 Aug 2017
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